Evolutionary comparison of the mechanism of DNA cleavage with respect to immune diversity and genomic instability

Biochemistry

Volumn 51, Issue 26, 2012, Pages 5243-5256

  Begum, Nasim A ^a   Honjo, Tasuku ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; DNA CLEAVAGE; EPIGENETIC MODIFICATION; EVOLUTIONARY PERSPECTIVE; GENETIC DISEASE; GENETIC MECHANISM; GENOMIC INSTABILITY; IMMUNOGLOBULIN GENES; MEIOTIC RECOMBINATIONS; SHEDDING LIGHT; SOMATIC HYPERMUTATION; SUPERCOILING; T LYMPHOCYTES; TARGET RECOGNITION; TOPOISOMERASES; TRIMETHYLATION;

DNA; ENZYMES; TRANSCRIPTION;

GENES;

B LYMPHOCYTE RECEPTOR; CYTIDINE DEAMINASE; DNA; HISTONE H3; RAG1 PROTEIN; RAG2 PROTEIN; T LYMPHOCYTE RECEPTOR;

ADAPTIVE IMMUNITY; ARTICLE; CHROMATIN; CLASS SWITCH RECOMBINATION; COMPARATIVE STUDY; DNA CLEAVAGE; DNA MODIFICATION; DNA RECOMBINATION; DNA SEQUENCE; DNA SUPERCOILING; EPIGENETICS; GENE MUTATION; GENETIC VARIABILITY; GENOMIC INSTABILITY; HISTONE METHYLATION; IMMUNOGLOBULIN GENE; MEIOSIS; MOLECULAR EVOLUTION; PRIORITY JOURNAL; RECOMBINATION SIGNAL SEQUENCE; SOMATIC HYPERMUTATION; TRANSCRIPTION ASSOCIATED MUTATION; TRANSCRIPTION INITIATION; VDJ RECOMBINATION; VERTEBRATE;

ANIMALS; CYTIDINE DEAMINASE; DNA CLEAVAGE; EVOLUTION, MOLECULAR; GENOMIC INSTABILITY; HUMANS; IMMUNOGLOBULIN CLASS SWITCHING; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN;

VERTEBRATA;

EID: 84863533953     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3005895     Document Type: Article

References (168)

1. Schatz, D. G. and Swanson, P. C. (2011) V(D)J recombination: Mechanisms of initiation Annu. Rev. Genet. 45, 167-202
2. Thompson, C. B. (1995) New insights into V(D)J recombination and its role in the evolution of the immune system Immunity 3, 531-539
3. Muramatsu, M., Kinoshita, K., Fagarasan, S., Yamada, S., Shinkai, Y., and Honjo, T. (2000) Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme Cell 102, 553-563
4. Muramatsu, M., Nagaoka, H., Shinkura, R., Begum, N. A., and Honjo, T. (2007) Discovery of activation-induced cytidine deaminase, the engraver of antibody memory Adv. Immunol. 94, 1-36
5. Rogozin, I. B., Iyer, L. M., Liang, L., Glazko, G. V., Liston, V. G., Pavlov, Y. I., Aravind, L., and Pancer, Z. (2007) Evolution and diversification of lamprey antigen receptors: Evidence for involvement of an AID-APOBEC family cytosine deaminase Nat. Immunol. 8, 647-656
6. Longerich, S. and Storb, U. (2005) The contested role of uracil DNA glycosylase in immunoglobulin gene diversification Trends Genet. 21, 253-256
7. Storb, U. and Stavnezer, J. (2002) Immunoglobulin genes: Generating diversity with AID and UNG Curr. Biol. 12, R725-R727
8. Aguilera, A. (2002) The connection between transcription and genomic instability EMBO J. 21, 195-201
9. La Spada, A. R. and Taylor, J. P. (2010) Repeat expansion disease: Progress and puzzles in disease pathogenesis Nat. Rev. Genet. 11, 247-258
10. Hubert, L., Jr., Lin, Y., Dion, V., and Wilson, J. H. (2011) Topoisomerase 1 and Single-Strand Break Repair Modulate Transcription-Induced CAG Repeat Contraction in Human Cells Mol. Cell. Biol. 31, 3105-3112
11. Lippert, M. J., Kim, N., Cho, J. E., Larson, R. P., Schoenly, N. E., O'Shea, S. H., and Jinks-Robertson, S. (2011) Role for topoisomerase 1 in transcription-associated mutagenesis in yeast Proc. Natl. Acad. Sci. U.S.A. 108, 698-703
12. Takahashi, T., Burguiere-Slezak, G., Van der Kemp, P. A., and Boiteux, S. (2011) Topoisomerase 1 provokes the formation of short deletions in repeated sequences upon high transcription in Saccharomyces cerevisiae Proc. Natl. Acad. Sci. U.S.A. 108, 692-697
13. Kobayashi, M., Sabouri, Z., Sabouri, S., Kitawaki, Y., Pommier, Y., Abe, T., Kiyonari, H., and Honjo, T. (2011) Decrease in topoisomerase I is responsible for activation-induced cytidine deaminase (AID)-dependent somatic hypermutation Proc. Natl. Acad. Sci. U.S.A. 108, 19305-19310
14. Kobayashi, M., Aida, M., Nagaoka, H., Begum, N. A., Kitawaki, Y., Nakata, M., Stanlie, A., Doi, T., Kato, L., Okazaki, I. M., Shinkura, R., Muramatsu, M., Kinoshita, K., and Honjo, T. (2009) AID-induced decrease in topoisomerase 1 induces DNA structural alteration and DNA cleavage for class switch recombination Proc. Natl. Acad. Sci. U.S.A. 106, 22375-22380
15. Gerton, J. L. and Hawley, R. S. (2005) Homologous chromosome interactions in meiosis: Diversity amidst conservation Nat. Rev. Genet. 6, 477-487
16. Baudat, F., Buard, J., Grey, C., Fledel-Alon, A., Ober, C., Przeworski, M., Coop, G., and de Massy, B. (2010) PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice Science 327, 836-840
17. Myers, S., Bowden, R., Tumian, A., Bontrop, R. E., Freeman, C., MacFie, T. S., McVean, G., and Donnelly, P. (2010) Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination Science 327, 876-879
18. Parvanov, E. D., Petkov, P. M., and Paigen, K. (2010) Prdm9 controls activation of mammalian recombination hotspots Science 327, 835
19. Pommier, Y. (2006) Topoisomerase I inhibitors: Camptothecins and beyond Nat. Rev. Cancer 6, 789-802
20. Zhao, J., Bacolla, A., Wang, G., and Vasquez, K. M. (2010) Non-B DNA structure-induced genetic instability and evolution Cell. Mol. Life Sci. 67, 43-62
21. Chuzhanova, N., Chen, J. M., Bacolla, A., Patrinos, G. P., Ferec, C., Wells, R. D., and Cooper, D. N. (2009) Gene conversion causing human inherited disease: Evidence for involvement of non-B-DNA-forming sequences and recombination-promoting motifs in DNA breakage and repair Hum. Mutat. 30, 1189-1198
22. Kim, N. and Jinks-Robertson, S. (2012) Transcription as a source of genome instability Nat. Rev. Genet. 13, 204-214
23. Petersen-Mahrt, S. K., Harris, R. S., and Neuberger, M. S. (2002) AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification Nature 418, 99-103
24. Chaudhuri, J., Tian, M., Khuong, C., Chua, K., Pinaud, E., and Alt, F. W. (2003) Transcription-targeted DNA deamination by the AID antibody diversification enzyme Nature 422, 726-730
25. Larson, E. D., Cummings, W. J., Bednarski, D. W., and Maizels, N. (2005) MRE11/RAD50 cleaves DNA in the AID/UNG-dependent pathway of immunoglobulin gene diversification Mol. Cell 20, 367-375
26. Okazaki, I. M., Hiai, H., Kakazu, N., Yamada, S., Muramatsu, M., Kinoshita, K., and Honjo, T. (2003) Constitutive expression of AID leads to tumorigenesis J. Exp. Med. 197, 1173-1181
27. Okazaki, I. M., Kotani, A., and Honjo, T. (2007) Role of AID in tumorigenesis Adv. Immunol. 94, 245-273
28. Schlissel, M. S. (2003) Regulating antigen-receptor gene assembly Nat. Rev. Immunol. 3, 890-899
29. Shimazaki, N., Tsai, A. G., and Lieber, M. R. (2009) H3K4me3 stimulates the V(D)J RAG complex for both nicking and hairpinning in trans in addition to tethering in cis: Implications for translocations Mol. Cell 34, 535-544
30. Grundy, G. J., Yang, W., and Gellert, M. (2010) Autoinhibition of DNA cleavage mediated by RAG1 and RAG2 is overcome by an epigenetic signal in V(D)J recombination Proc. Natl. Acad. Sci. U.S.A. 107, 22487-22492
31. Curry, J. D., Schulz, D., Guidos, C. J., Danska, J. S., Nutter, L., Nussenzweig, A., and Schlissel, M. S. (2007) Chromosomal reinsertion of broken RSS ends during T cell development J. Exp. Med. 204, 2293-2303
32. Marculescu, R., Vanura, K., Montpellier, B., Roulland, S., Le, T., Navarro, J. M., Jager, U., McBlane, F., and Nadel, B. (2006) Recombinase, chromosomal translocations and lymphoid neoplasia: Targeting mistakes and repair failures DNA Repair 5, 1246-1258
33. Keeney, S., Giroux, C. N., and Kleckner, N. (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family Cell 88, 375-384
34. Keeney, S. (2008) Spo11 and the Formation of DNA Double-Strand Breaks in Meiosis Genome Dynamics and Stability 2, 81-123
35. Hartsuiker, E., Mizuno, K., Molnar, M., Kohli, J., Ohta, K., and Carr, A. M. (2009) Ctp1CtIP and Rad32Mre11 nuclease activity are required for Rec12Spo11 removal, but Rec12Spo11 removal is dispensable for other MRN-dependent meiotic functions Mol. Cell. Biol. 29, 1671-1681
36. Wang, A. J., Quigley, G. J., Kolpak, F. J., van der Marel, G., van Boom, J. H., and Rich, A. (1981) Left-handed double helical DNA: Variations in the backbone conformation Science 211, 171-176
37. Wang, G. and Vasquez, K. M. (2006) Non-B DNA structure-induced genetic instability Mutat. Res. 598, 103-119
38. Nambiar, M., Kari, V., and Raghavan, S. C. (2008) Chromosomal translocations in cancer Biochim. Biophys. Acta 1786, 139-152
39. Nambiar, M. and Raghavan, S. C. (2011) How does DNA break during chromosomal translocations? Nucleic Acids Res. 39, 5813-5825
40. Michelotti, G. A., Michelotti, E. F., Pullner, A., Duncan, R. C., Eick, D., and Levens, D. (1996) Multiple single-stranded cis elements are associated with activated chromatin of the human c-myc gene in vivo Mol. Cell. Biol. 16, 2656-2669
41. Raghavan, S. C., Chastain, P., Lee, J. S., Hegde, B. G., Houston, S., Langen, R., Hsieh, C. L., Haworth, I. S., and Lieber, M. R. (2005) Evidence for a triplex DNA conformation at the bcl-2 major breakpoint region of the t(14;18) translocation J. Biol. Chem. 280, 22749-22760
42. Raghavan, S. C., Swanson, P. C., Wu, X., Hsieh, C. L., and Lieber, M. R. (2004) A non-B-DNA structure at the Bcl-2 major breakpoint region is cleaved by the RAG complex Nature 428, 88-93
43. Wang, G., Carbajal, S., Vijg, J., DiGiovanni, J., and Vasquez, K. M. (2008) DNA structure-induced genomic instability in vivo J. Natl. Cancer Inst. 100, 1815-1817
44. Wells, R. D. (1996) Molecular basis of genetic instability of triplet repeats J. Biol. Chem. 271, 2875-2878
45. Wojciechowska, M., Napierala, M., Larson, J. E., and Wells, R. D. (2006) Non-B DNA conformations formed by long repeating tracts of myotonic dystrophy type 1, myotonic dystrophy type 2, and Friedreich's ataxia genes, not the sequences per se, promote mutagenesis in flanking regions J. Biol. Chem. 281, 24531-24543
46. Napierala, M., Bacolla, A., and Wells, R. D. (2005) Increased negative superhelical density in vivo enhances the genetic instability of triplet repeat sequences J. Biol. Chem. 280, 37366-37376
47. Tsao, Y. P., Wu, H. Y., and Liu, L. F. (1989) Transcription-driven supercoiling of DNA: Direct biochemical evidence from in vitro studies Cell 56, 111-118
48. Albert, A. C., Spirito, F., Figueroa-Bossi, N., Bossi, L., and Rahmouni, A. R. (1996) Hyper-negative template DNA supercoiling during transcription of the tetracycline-resistance gene in topA mutants is largely constrained in vivo Nucleic Acids Res. 24, 3093-3099
49. Bacolla, A., Gellibolian, R., Shimizu, M., Amirhaeri, S., Kang, S., Ohshima, K., Larson, J. E., Harvey, S. C., Stollar, B. D., and Wells, R. D. (1997) Flexible DNA: Genetically unstable CTG.CAG and CGG.CCG from human hereditary neuromuscular disease genes J. Biol. Chem. 272, 16783-16792
50. Kozlowski, P., Sobczak, K., and Krzyzosiak, W. J. (2010) Trinucleotide repeats: Triggers for genomic disorders? Genome Med. 2, 29
51. Crespan, E., Czabany, T., Maga, G., and Hubscher, U. (2012) Microhomology-mediated DNA strand annealing and elongation by human DNA polymerases λ and β on normal and repetitive DNA sequences Nucleic Acids Res. DOI: 10.1093/nar/gks186
52. Nakamori, M., Pearson, C. E., and Thornton, C. A. (2011) Bidirectional transcription stimulates expansion and contraction of expanded (CTG)*(CAG) repeats Hum. Mol. Genet. 20, 580-588
53. El Hage, A., French, S. L., Beyer, A. L., and Tollervey, D. (2010) Loss of topoisomerase I leads to R-loop-mediated transcriptional blocks during ribosomal RNA synthesis Genes Dev. 24, 1546-1558
54. Lin, Y., Dent, S. Y., Wilson, J. H., Wells, R. D., and Napierala, M. (2010) R loops stimulate genetic instability of CTG.CAG repeats Proc. Natl. Acad. Sci. U.S.A. 107, 692-697
55. Tian, M. and Alt, F. W. (2000) Transcription-induced cleavage of immunoglobulin switch regions by nucleotide excision repair nucleases in vitro J. Biol. Chem. 275, 24163-24172
56. Perlot, T., Li, G., and Alt, F. W. (2008) Antisense transcripts from immunoglobulin heavy-chain locus V(D)J and switch regions Proc. Natl. Acad. Sci. U.S.A. 105, 3843-3848
57. Huang, F. T., Yu, K., Balter, B. B., Selsing, E., Oruc, Z., Khamlichi, A. A., Hsieh, C. L., and Lieber, M. R. (2007) Sequence dependence of chromosomal R-loops at the immunoglobulin heavy-chain Smu class switch region Mol. Cell. Biol. 27, 5921-5932
58. Haddad, D., Oruc, Z., Puget, N., Laviolette-Malirat, N., Philippe, M., Carrion, C., Le Bert, M., and Khamlichi, A. A. (2011) Sense transcription through the S region is essential for immunoglobulin class switch recombination EMBO J. 30, 1608-1620
59. Yan, C. T., Boboila, C., Souza, E. K., Franco, S., Hickernell, T. R., Murphy, M., Gumaste, S., Geyer, M., Zarrin, A. A., Manis, J. P., Rajewsky, K., and Alt, F. W. (2007) IgH class switching and translocations use a robust non-classical end-joining pathway Nature 449, 478-482
60. Rooney, S., Chaudhuri, J., and Alt, F. W. (2004) The role of the non-homologous end-joining pathway in lymphocyte development Immunol. Rev. 200, 115-131
61. Stavnezer, J., Kinoshita, K., Muramatsu, M., and Honjo, T. (2004) Chapter 20: Molecular mechanism of class switch recombination. In Molecular Biology of B Cells (Honjo, T., Alt, F. W., and Neuberger, M. S., Eds.) pp 307-326, Elsevier Ltd., Amsterdam.
62. Dunnick, W., Hertz, G. Z., Scappino, L., and Gritzmacher, C. (1993) DNA sequences at immunoglobulin switch region recombination sites Nucleic Acids Res. 21, 365-372
63. Luby, T. M., Schrader, C. E., Stavnezer, J., and Selsing, E. (2001) The mu switch region tandem repeats are important, but not required, for antibody class switch recombination J. Exp. Med. 193, 159-168
64. Harriman, G. R., Bradley, A., Das, S., Rogers-Fani, P., and Davis, A. C. (1996) IgA class switch in Iα exon-deficient mice. Role of germline transcription in class switch recombination J. Clin. Invest. 97, 477-485
65. Xu, L., Gorham, B., Li, S. C., Bottaro, A., Alt, F. W., and Rothman, P. (1993) Replacement of germ-line ε promoter by gene targeting alters control of immunoglobulin heavy chain class switching Proc. Natl. Acad. Sci. U.S.A. 90, 3705-3709
66. Oruc, Z., Boumediene, A., Le Bert, M., and Khamlichi, A. A. (2007) Replacement of Iγ3 germ-line promoter by Iγ1 inhibits class-switch recombination to IgG3 Proc. Natl. Acad. Sci. U.S.A. 104, 20484-20489
67. Zarrin, A. A., Alt, F. W., Chaudhuri, J., Stokes, N., Kaushal, D., Du Pasquier, L., and Tian, M. (2004) An evolutionarily conserved target motif for immunoglobulin class-switch recombination Nat. Immunol. 5, 1275-1281
68. Shinkura, R., Tian, M., Smith, M., Chua, K., Fujiwara, Y., and Alt, F. W. (2003) The influence of transcriptional orientation on endogenous switch region function Nat. Immunol. 4, 435-441
69. Han, L., Masani, S., and Yu, K. (2011) Overlapping activation-induced cytidine deaminase hotspot motifs in Ig class-switch recombination Proc. Natl. Acad. Sci. U.S.A. 108, 11584-11589
70. Raghavan, S. C., Tsai, A., Hsieh, C. L., and Lieber, M. R. (2006) Analysis of non-B DNA structure at chromosomal sites in the mammalian genome Methods Enzymol. 409, 301-316
71. Nambiar, M., Goldsmith, G., Moorthy, B. T., Lieber, M. R., Joshi, M. V., Choudhary, B., Hosur, R. V., and Raghavan, S. C. (2011) Formation of a G-quadruplex at the BCL2 major breakpoint region of the t(14;18) translocation in follicular lymphoma Nucleic Acids Res. 39, 936-948
72. Fukita, Y., Jacobs, H., and Rajewsky, K. (1998) Somatic hypermutation in the heavy chain locus correlates with transcription Immunity 9, 105-114
73. Storb, U., Peters, A., Klotz, E., Rogerson, B., and Hackett, J., Jr. (1996) The mechanism of somatic hypermutation studied with transgenic and transfected target genes Semin. Immunol. 8, 131-140
74. Peters, A. and Storb, U. (1996) Somatic hypermutation of immunoglobulin genes is linked to transcription initiation Immunity 4, 57-65
75. Bachl, J., Carlson, C., Gray-Schopfer, V., Dessing, M., and Olsson, C. (2001) Increased transcription levels induce higher mutation rates in a hypermutating cell line J. Immunol. 166, 5051-5057
76. Peled, J. U., Kuang, F. L., Iglesias-Ussel, M. D., Roa, S., Kalis, S. L., Goodman, M. F., and Scharff, M. D. (2008) The biochemistry of somatic hypermutation Annu. Rev. Immunol. 26, 481-511
77. Winter, D. B. and Gearhart, P. J. (1998) Dual enigma of somatic hypermutation of immunoglobulin variable genes: Targeting and mechanism Immunol. Rev. 162, 89-96
78. Lebecque, S. G. and Gearhart, P. J. (1990) Boundaries of somatic mutation in rearranged immunoglobulin genes: 5′ boundary is near the promoter, and 3′ boundary is approximately 1 kb from V(D)J gene J. Exp. Med. 172, 1717-1727
79. Ronai, D., Iglesias-Ussel, M. D., Fan, M., Li, Z., Martin, A., and Scharff, M. D. (2007) Detection of chromatin-associated single-stranded DNA in regions targeted for somatic hypermutation J. Exp. Med. 204, 181-190
80. Parsa, J. Y., Ramachandran, S., Zaheen, A., Nepal, R. M., Kapelnikov, A., Belcheva, A., Berru, M., Ronai, D., and Martin, A. (2012) Negative Supercoiling Creates Single-Stranded Patches of DNA That Are Substrates for AID-Mediated Mutagenesis PLoS Genet. 8, e1002518
81. Wright, B. E., Schmidt, K. H., Davis, N., Hunt, A. T., and Minnick, M. F. (2008) II. Correlations between secondary structure stability and mutation frequency during somatic hypermutation Mol. Immunol. 45, 3600-3608
82. Wright, B. E., Schmidt, K. H., Minnick, M. F., and Davis, N. (2008) I. VH gene transcription creates stabilized secondary structures for coordinated mutagenesis during somatic hypermutation Mol. Immunol. 45, 3589-3599
83. Shapiro, G. S., Aviszus, K., Ikle, D., and Wysocki, L. J. (1999) Predicting regional mutability in antibody V genes based solely on di- and trinucleotide sequence composition J. Immunol. 163, 259-268
84. Smith, D. S., Creadon, G., Jena, P. K., Portanova, J. P., Kotzin, B. L., and Wysocki, L. J. (1996) Di- and trinucleotide target preferences of somatic mutagenesis in normal and autoreactive B cells J. Immunol. 156, 2642-2652
85. Michael, N., Shen, H. M., Longerich, S., Kim, N., Longacre, A., and Storb, U. (2003) The E box motif CAGGTG enhances somatic hypermutation without enhancing transcription Immunity 19, 235-242
86. Bachl, J. and Olsson, C. (1999) Hypermutation targets a green fluorescent protein-encoding transgene in the presence of immunoglobulin enhancers Eur. J. Immunol. 29, 1383-1389
87. Yoshikawa, K., Okazaki, I. M., Eto, T., Kinoshita, K., Muramatsu, M., Nagaoka, H., and Honjo, T. (2002) AID enzyme-induced hypermutation in an actively transcribed gene in fibroblasts Science 296, 2033-2036
88. Pham, P., Bransteitter, R., Petruska, J., and Goodman, M. F. (2003) Processive AID-catalysed cytosine deamination on single-stranded DNA simulates somatic hypermutation Nature 424, 103-107
89. Michael, N., Martin, T. E., Nicolae, D., Kim, N., Padjen, K., Zhan, P., Nguyen, H., Pinkert, C., and Storb, U. (2002) Effects of sequence and structure on the hypermutability of immunoglobulin genes Immunity 16, 123-134
90. Faili, A., Aoufouchi, S., Gueranger, Q., Zober, C., Leon, A., Bertocci, B., Weill, J. C., and Reynaud, C. A. (2002) AID-dependent somatic hypermutation occurs as a DNA single-strand event in the BL2 cell line Nat. Immunol. 3, 815-821
91. Bemark, M. and Neuberger, M. S. (2000) The c-MYC allele that is translocated into the IgH locus undergoes constitutive hypermutation in a Burkitt's lymphoma line Oncogene 19, 3404-3410
92. Kato, L., Begum, N. A., Burroughs, A. M., Doi, T., Kawai, J., Daub, C. O., Kawaguchi, T., Matsuda, F., Hayashizaki, Y., and Honjo, T. (2012) Nonimmunoglobulin target loci of activation-induced cytidine deaminase (AID) share unique features with immunoglobulin genes Proc. Natl. Acad. Sci. U.S.A. 109, 2479-2484
93. Yu, K., Chedin, F., Hsieh, C. L., Wilson, T. E., and Lieber, M. R. (2003) R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells Nat. Immunol. 4, 442-451
94. Kim, N. and Jinks-Robertson, S. (2011) Guanine repeat-containing sequences confer transcription-dependent instability in an orientation-specific manner in yeast DNA Repair 10, 953-960
95. Dominguez Sanchez, M. S., Barroso, S., Gomez-Gonzalez, B., Luna, R., and Aguilera, A. (2011) Genome instability and transcription elongation impairment in human cells depleted of THO/TREX PLoS Genet. 7, e1002386
96. Bransteitter, R., Pham, P., Scharff, M. D., and Goodman, M. F. (2003) Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase Proc. Natl. Acad. Sci. U.S.A. 100, 4102-4107
97. Yu, K., Roy, D., Bayramyan, M., Haworth, I. S., and Lieber, M. R. (2005) Fine-structure analysis of activation-induced deaminase accessibility to class switch region R-loops Mol. Cell. Biol. 25, 1730-1736
98. Lee, C. G., Kinoshita, K., Arudchandran, A., Cerritelli, S. M., Crouch, R. J., and Honjo, T. (2001) Quantitative regulation of class switch recombination by switch region transcription J. Exp. Med. 194, 365-374
99. Basu, U., Meng, F. L., Keim, C., Grinstein, V., Pefanis, E., Eccleston, J., Zhang, T., Myers, D., Wasserman, C. R., Wesemann, D. R., Januszyk, K., Gregory, R. I., Deng, H., Lima, C. D., and Alt, F. W. (2011) The RNA exosome targets the AID cytidine deaminase to both strands of transcribed duplex DNA substrates Cell 144, 353-363
100. Dominguez-Sanchez, M. S., Barroso, S., Gomez-Gonzalez, B., Luna, R., and Aguilera, A. (2011) Genome instability and transcription elongation impairment in human cells depleted of THO/TREX PLoS Genet. 7, e1002386
101. Mischo, H. E., Gomez-Gonzalez, B., Grzechnik, P., Rondon, A. G., Wei, W., Steinmetz, L., Aguilera, A., and Proudfoot, N. J. (2011) Yeast Sen1 helicase protects the genome from transcription-associated instability Mol. Cell 41, 21-32
102. Skourti-Stathaki, K., Proudfoot, N. J., and Gromak, N. (2011) Human senataxin resolves RNA/DNA hybrids formed at transcriptional pause sites to promote Xrn2-dependent termination Mol. Cell 42, 794-805
103. Basu, U., Chaudhuri, J., Alpert, C., Dutt, S., Ranganath, S., Li, G., Schrum, J. P., Manis, J. P., and Alt, F. W. (2005) The AID antibody diversification enzyme is regulated by protein kinase A phosphorylation Nature 438, 508-511
104. Chaudhuri, J., Khuong, C., and Alt, F. W. (2004) Replication protein A interacts with AID to promote deamination of somatic hypermutation targets Nature 430, 992-998
105. Jeevan-Raj, B. P., Robert, I., Heyer, V., Page, A., Wang, J. H., Cammas, F., Alt, F. W., Losson, R., and Reina-San-Martin, B. (2011) Epigenetic tethering of AID to the donor switch region during immunoglobulin class switch recombination J. Exp. Med. 208, 1649-1660
106. MacDuff, D. A., Neuberger, M. S., and Harris, R. S. (2006) MDM2 can interact with the C-terminus of AID but it is inessential for antibody diversification in DT40 B cells Mol. Immunol. 43, 1099-1108
107. Nambu, Y., Sugai, M., Gonda, H., Lee, C. G., Katakai, T., Agata, Y., Yokota, Y., and Shimizu, A. (2003) Transcription-coupled events associating with immunoglobulin switch region chromatin Science 302, 2137-2140
108. Okazaki, I. M., Okawa, K., Kobayashi, M., Yoshikawa, K., Kawamoto, S., Nagaoka, H., Shinkura, R., Kitawaki, Y., Taniguchi, H., Natsume, T., Iemura, S., and Honjo, T. (2011) Histone chaperone Spt6 is required for class switch recombination but not somatic hypermutation Proc. Natl. Acad. Sci. U.S.A. 108, 7920-7925
109. Pasqualucci, L., Kitaura, Y., Gu, H., and Dalla-Favera, R. (2006) PKA-mediated phosphorylation regulates the function of activation-induced deaminase (AID) in B cells Proc. Natl. Acad. Sci. U.S.A. 103, 395-400
110. Pavri, R., Gazumyan, A., Jankovic, M., Di Virgilio, M., Klein, I., Ansarah-Sobrinho, C., Resch, W., Yamane, A., Reina San-Martin, B., Barreto, V., Nieland, T. J., Root, D. E., Casellas, R., and Nussenzweig, M. C. (2010) Activation-induced cytidine deaminase targets DNA at sites of RNA polymerase II stalling by interaction with Spt5 Cell 143, 122-133
111. Wu, X., Geraldes, P., Platt, J. L., and Cascalho, M. (2005) The double-edged sword of activation-induced cytidine deaminase J. Immunol. 174, 934-941
112. Ta, V. T., Nagaoka, H., Catalan, N., Durandy, A., Fischer, A., Imai, K., Nonoyama, S., Tashiro, J., Ikegawa, M., Ito, S., Kinoshita, K., Muramatsu, M., and Honjo, T. (2003) AID mutant analyses indicate requirement for class-switch-specific cofactors Nat. Immunol. 4, 843-848
113. Barreto, V. M. and Magor, B. G. (2011) Activation-induced cytidine deaminase structure and functions: A species comparative view Dev. Comp. Immunol. 35, 991-1007
114. Wakae, K., Magor, B. G., Saunders, H., Nagaoka, H., Kawamura, A., Kinoshita, K., Honjo, T., and Muramatsu, M. (2006) Evolution of class switch recombination function in fish activation-induced cytidine deaminase, AID Int. Immunol. 18, 41-47
115. Chaudhuri, J. and Alt, F. W. (2004) Class-switch recombination: Interplay of transcription, DNA deamination and DNA repair Nat. Rev. Immunol. 4, 541-552
116. Hasler, J., Rada, C., and Neuberger, M. S. (2011) Cytoplasmic activation-induced cytidine deaminase (AID) exists in stoichiometric complex with translation elongation factor 1α (eEF1A) Proc. Natl. Acad. Sci. U.S.A. 108, 18366-18371
117. Durandy, A., Peron, S., Taubenheim, N., and Fischer, A. (2006) Activation-induced cytidine deaminase: Structure-function relationship as based on the study of mutants Hum. Mutat. 27, 1185-1191
118. Doi, T., Kato, L., Ito, S., Shinkura, R., Wei, M., Nagaoka, H., Wang, J., and Honjo, T. (2009) The C-terminal region of activation-induced cytidine deaminase is responsible for a recombination function other than DNA cleavage in class switch recombination Proc. Natl. Acad. Sci. U.S.A. 106, 2758-2763
119. Abarrategui, I. and Krangel, M. S. (2006) Regulation of T cell receptor-α gene recombination by transcription Nat. Immunol. 7, 1109-1115
120. Jung, D., Giallourakis, C., Mostoslavsky, R., and Alt, F. W. (2006) Mechanism and control of V(D)J recombination at the immunoglobulin heavy chain locus Annu. Rev. Immunol. 24, 541-570
121. Bassing, C. H., Swat, W., and Alt, F. W. (2002) The mechanism and regulation of chromosomal V(D)J recombination Cell 109 (Suppl.) S45-S55
122. Sakano, H., Huppi, K., Heinrich, G., and Tonegawa, S. (1979) Sequences at the somatic recombination sites of immunoglobulin light-chain genes Nature 280, 288-294
123. Rahman, N. S., Godderz, L. J., Stray, S. J., Capra, J. D., and Rodgers, K. K. (2006) DNA cleavage of a cryptic recombination signal sequence by RAG1 and RAG2. Implications for partial V(H) gene replacement J. Biol. Chem. 281, 12370-12380
124. Zhang, M. and Swanson, P. C. (2008) V(D)J recombinase binding and cleavage of cryptic recombination signal sequences identified from lymphoid malignancies J. Biol. Chem. 283, 6717-6727
125. Lee, A. I., Fugmann, S. D., Cowell, L. G., Ptaszek, L. M., Kelsoe, G., and Schatz, D. G. (2003) A functional analysis of the spacer of V(D)J recombination signal sequences PLoS Biol. 1, E1
126. Schatz, D. G. and Ji, Y. (2011) Recombination centres and the orchestration of V(D)J recombination Nat. Rev. Immunol. 11, 251-263
127. Kapitonov, V. V. and Jurka, J. (2005) RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons PLoS Biol. 3, e181
128. Marculescu, R., Le, T., Simon, P., Jaeger, U., and Nadel, B. (2002) V(D)J-mediated translocations in lymphoid neoplasms: A functional assessment of genomic instability by cryptic sites J. Exp. Med. 195, 85-98
129. Nambiar, M. and Raghavan, S. C. (2012) Mechanism of Fragility at BCL2 Gene Minor Breakpoint Cluster Region during t(14;18) Chromosomal Translocation J. Biol. Chem. 287, 8688-8701
130. Mahowald, G. K., Baron, J. M., and Sleckman, B. P. (2008) Collateral damage from antigen receptor gene diversification Cell 135, 1009-1012
131. Tsai, A. G., Lu, H., Raghavan, S. C., Muschen, M., Hsieh, C. L., and Lieber, M. R. (2008) Human chromosomal translocations at CpG sites and a theoretical basis for their lineage and stage specificity Cell 135, 1130-1142
132. Arnheim, N., Calabrese, P., and Tiemann-Boege, I. (2007) Mammalian meiotic recombination hot spots Annu. Rev. Genet. 41, 369-399
133. Smagulova, F., Gregoretti, I. V., Brick, K., Khil, P., Camerini-Otero, R. D., and Petukhova, G. V. (2011) Genome-wide analysis reveals novel molecular features of mouse recombination hotspots Nature 472, 375-378
134. Mihola, O., Trachtulec, Z., Vlcek, C., Schimenti, J. C., and Forejt, J. (2009) A mouse speciation gene encodes a meiotic histone H3 methyltransferase Science 323, 373-375
135. Wahls, W. P. and Davidson, M. K. (2010) Discrete DNA sites regulate global distribution of meiotic recombination Trends Genet. 26, 202-208
136. Wahls, W. P. and Davidson, M. K. (2011) DNA sequence-mediated, evolutionarily rapid redistribution of meiotic recombination hotspots Genetics 189, 685-694
137. Borde, V., Robine, N., Lin, W., Bonfils, S., Geli, V., and Nicolas, A. (2009) Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites EMBO J. 28, 99-111
138. Stanlie, A., Aida, M., Muramatsu, M., Honjo, T., and Begum, N. A. (2010) Histone3 lysine4 trimethylation regulated by the facilitates chromatin transcription complex is critical for DNA cleavage in class switch recombination Proc. Natl. Acad. Sci. U.S.A. 107, 22190-22195
139. Matthews, A. G., Kuo, A. J., Ramon-Maiques, S., Han, S., Champagne, K. S., Ivanov, D., Gallardo, M., Carney, D., Cheung, P., Ciccone, D. N., Walter, K. L., Utz, P. J., Shi, Y., Kutateladze, T. G., Yang, W., Gozani, O., and Oettinger, M. A. (2007) RAG2 PHD finger couples histone H3 lysine 4 trimethylation with V(D)J recombination Nature 450, 1106-1110
140. Trievel, R. C. and Shilatifard, A. (2009) WDR5, a complexed protein Nat. Struct. Mol. Biol. 16, 678-680
141. Sollier, J., Lin, W., Soustelle, C., Suhre, K., Nicolas, A., Geli, V., and de La Roche Saint-Andre, C. (2004) Set1 is required for meiotic S-phase onset, double-strand break formation and middle gene expression EMBO J. 23, 1957-1967
142. Weake, V. M. and Workman, J. L. (2008) Histone ubiquitination: Triggering gene activity Mol. Cell 29, 653-663
143. Chen, Y., Yamaguchi, Y., Tsugeno, Y., Yamamoto, J., Yamada, T., Nakamura, M., Hisatake, K., and Handa, H. (2009) DSIF, the Paf1 complex, and Tat-SF1 have nonredundant, cooperative roles in RNA polymerase II elongation Genes Dev. 23, 2765-2777
144. Chandrasekharan, M. B., Huang, F., and Sun, Z. W. (2010) Histone H2B ubiquitination and beyond: Regulation of nucleosome stability, chromatin dynamics and the trans-histone H3 methylation Epigenetics 5, 460-468
145. Stanlie, A., Begum, N. A., Akiyama, H., and Honjo, T. (2012) The DSIF Subunits Spt4 and Spt5 Have Distinct Roles at Various Phases of Immunoglobulin Class Switch Recombination PLoS Genet. 8, e1002675
146. Zhou, K., Kuo, W. H., Fillingham, J., and Greenblatt, J. F. (2009) Control of transcriptional elongation and cotranscriptional histone modification by the yeast BUR kinase substrate Spt5 Proc. Natl. Acad. Sci. U.S.A. 106, 6956-6961
147. Begum, N. A., Stanlie, A. S., Akiyama, H., and Honjo, T. (2012) The histone chaperone SPT6 is required for AID Target determination through H3K4me3 regulation, submitted for publication.
148. Klein, I. A., Resch, W., Jankovic, M., Oliveira, T., Yamane, A., Nakahashi, H., Di Virgilio, M., Bothmer, A., Nussenzweig, A., Robbiani, D. F., Casellas, R., and Nussenzweig, M. C. (2011) Translocation-capture sequencing reveals the extent and nature of chromosomal rearrangements in B lymphocytes Cell 147, 95-106
149. Wang, L., Wuerffel, R., Feldman, S., Khamlichi, A. A., and Kenter, A. L. (2009) S region sequence, RNA polymerase II, and histone modifications create chromatin accessibility during class switch recombination J. Exp. Med. 206, 1817-1830
150. Yamane, A., Resch, W., Kuo, N., Kuchen, S., Li, Z., Sun, H. W., Robbiani, D. F., McBride, K., Nussenzweig, M. C., and Casellas, R. (2011) Deep-sequencing identification of the genomic targets of the cytidine deaminase AID and its cofactor RPA in B lymphocytes Nat. Immunol. 12, 62-69
151. Buard, J., Barthes, P., Grey, C., and de Massy, B. (2009) Distinct histone modifications define initiation and repair of meiotic recombination in the mouse EMBO J. 28, 2616-2624
152. Brinkman, A. B., Roelofsen, T., Pennings, S. W., Martens, J. H., Jenuwein, T., and Stunnenberg, H. G. (2006) Histone modification patterns associated with the human X chromosome EMBO Rep. 7, 628-634
153. Vakoc, C. R., Mandat, S. A., Olenchock, B. A., and Blobel, G. A. (2005) Histone H3 lysine 9 methylation and HP1γ are associated with transcription elongation through mammalian chromatin Mol. Cell 19, 381-391
154. Daniel, J. A., Santos, M. A., Wang, Z., Zang, C., Schwab, K. R., Jankovic, M., Filsuf, D., Chen, H. T., Gazumyan, A., Yamane, A., Cho, Y. W., Sun, H. W., Ge, K., Peng, W., Nussenzweig, M. C., Casellas, R., Dressler, G. R., Zhao, K., and Nussenzweig, A. (2010) PTIP promotes chromatin changes critical for immunoglobulin class switch recombination Science 329, 917-923
155. McBlane, F. and Boyes, J. (2000) Stimulation of V(D)J recombination by histone acetylation Curr. Biol. 10, 483-486
156. McMurry, M. T. and Krangel, M. S. (2000) A role for histone acetylation in the developmental regulation of VDJ recombination Science 287, 495-498
157. Roth, D. B. and Roth, S. Y. (2000) Unequal access: Regulating V(D)J recombination through chromatin remodeling Cell 103, 699-702
158. Du, H., Ishii, H., Pazin, M. J., and Sen, R. (2008) Activation of 12/23-RSS-dependent RAG cleavage by hSWI/SNF complex in the absence of transcription Mol. Cell 31, 641-649
159. Liu, Y., Subrahmanyam, R., Chakraborty, T., Sen, R., and Desiderio, S. (2007) A plant homeodomain in RAG-2 that binds hypermethylated lysine 4 of histone H3 is necessary for efficient antigen-receptor-gene rearrangement Immunity 27, 561-571
160. Ramon-Maiques, S., Kuo, A. J., Carney, D., Matthews, A. G., Oettinger, M. A., Gozani, O., and Yang, W. (2007) The plant homeodomain finger of RAG2 recognizes histone H3 methylated at both lysine-4 and arginine-2 Proc. Natl. Acad. Sci. U.S.A. 104, 18993-18998
161. Villa, A., Sobacchi, C., and Vezzoni, P. (2002) Omenn syndrome in the context of other B cell-negative severe combined immunodeficiencies Isr. Med. Assoc. J. 4, 218-221
162. Kniewel, R. and Keeney, S. (2009) Histone methylation sets the stage for meiotic DNA breaks EMBO J. 28, 81-83
163. Grey, C., Barthes, P., Chauveau-Le Friec, G., Langa, F., Baudat, F., and de Massy, B. (2011) Mouse PRDM9 DNA-binding specificity determines sites of histone H3 lysine 4 trimethylation for initiation of meiotic recombination PLoS Biol. 9, e1001176
164. Ng, H. H., Robert, F., Young, R. A., and Struhl, K. (2003) Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity Mol. Cell 11, 709-719
165. Ponting, C. P. (2011) What are the genomic drivers of the rapid evolution of PRDM9? Trends Genet. 27, 165-171
166. Segurel, L., Leffler, E. M., and Przeworski, M. (2011) The case of the fickle fingers: how the PRDM9 zinc finger protein specifies meiotic recombination hotspots in humans PLoS Biol. 9, e1001211
167. Getun, I. V., Wu, Z. K., Khalil, A. M., and Bois, P. R. (2010) Nucleosome occupancy landscape and dynamics at mouse recombination hotspots EMBO Rep. 11, 555-560
168. Wu, Z. K., Getun, I. V., and Bois, P. R. (2010) Anatomy of mouse recombination hot spots Nucleic Acids Res. 38, 2346-2354